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ORIGINAL ARTICLE DNA Barcoding British Euphrasia Reveals

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ORIGINAL ARTICLE DNA Barcoding British Euphrasia Reveals bioRxiv preprint doi: https://doi.org/10.1101/164681; this version posted July 17, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 ORIGINAL ARTICLE 2 DNA barcoding British Euphrasia reveals deeply divergent polyploids but lack of 3 species-level resolution 4 Xumei Wang1, Galina Gussarova2,3,4, Markus Ruhsam5, Natasha de Vere6, Chris Metherell7, 5 Peter M. Hollingsworth5, Alex D. Twyford8* 6 1 School of Pharmacy, Xi'an Jiaotong University, 76 Yanta West Road, Xi'an, 710061, 7 P.R.China 8 2 Tromsø University Museum, UiT The Arctic University of Norway, PO box 6050 Langnes, 9 NO-9037, Tromsø, Norway 10 3 CEES-Centre for Ecological and Evolutionary Synthesis, Dept. of Biosciences, University 11 of Oslo, PO BOX 1066, Blindern, NO-0316, Norway 12 4 Dept. of Botany, Faculty of Biology, St Petersburg State University, Universitetskaya nab. 13 7/9, 199034 St Petersburg, Russia 14 5 Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK 15 6 National Botanic Garden of Wales, Llanarthne, Carmarthenshire, SA32 8HG, UK and 16 Institute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, 17 Penglais, Aberystwyth, Ceredigion, SY23 3DA, UK 18 7 57 Walton Rd, Bristol BS11 9TA 19 8 University of Edinburgh, Institute of Evolutionary Biology, West Mains Road, Edinburgh, 20 EH3 9JT, UK 21 22 Running title: Complex patterns of diversity in Euphrasia 23 For correspondence: [email protected] 24 1 bioRxiv preprint doi: https://doi.org/10.1101/164681; this version posted July 17, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 25 26 ABSTRACT 27 Background and aims DNA barcoding is emerging as a useful tool not only for species 28 identification but for studying evolutionary and ecological processes. Although plant DNA 29 barcodes do not always provide species-level resolution, the generation of large DNA 30 barcode datasets can provide insights into the mechanisms underlying the generation of 31 species diversity. Here, we use DNA barcoding to study evolutionary processes in 32 taxonomically complex British Euphrasia, a group with multiple ploidy levels, frequent self- 33 fertilization, young species divergence and widespread hybridisation. 34 Methods We sequenced the core plant barcoding loci, supplemented with additional nuclear 35 and plastid loci, in representatives of all 19 British Euphrasia species. We analyse these data 36 in a population genetic and phylogenetic framework. We then date the divergence of 37 haplotypes in a global Euphrasia dataset using a time-calibrated Bayesian approach 38 implemented in BEAST. 39 Key results No Euphrasia species has a consistent diagnostic haplotype. Instead, haplotypes 40 are either widespread across species, or are population specific. Nuclear genetic variation is 41 strongly partitioned by ploidy levels, with diploid and tetraploid British Euphrasia possessing 42 deeply divergent ITS haplotypes (DXY = 5.1%), with haplotype divergence corresponding to 43 the late Miocene. In contrast, plastid data show no clear division by ploidy, and instead reveal 44 weakly supported geographic patterns. 45 Conclusions Using standard DNA barcoding loci for species identification in Euphrasia will 46 be unsuccessful. However, these loci provide key insights into the maintenance of genetic 47 variation, with divergence of diploids and tetraploids suggesting that ploidy differences act as 48 a barrier to gene exchange in British Euphrasia, with rampant hybridisation within ploidy 49 levels. The scarcity of shared diploid-tetraploid ITS haplotypes supports the polyploids being 2 bioRxiv preprint doi: https://doi.org/10.1101/164681; this version posted July 17, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 50 allotetraploid in origin. Overall, these results show that even when lacking species-level 51 resolution, DNA barcoding can reveal insightful evolutionary patterns in taxonomically 52 complex genera. 53 54 Keywords: DNA barcoding, Euphrasia, Orobanchaceae, polyploidy, taxonomic complexity, 55 British flora, phylogeny 56 3 bioRxiv preprint doi: https://doi.org/10.1101/164681; this version posted July 17, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 57 58 INTRODUCTION 59 60 DNA barcoding is a valuable tool for discriminating among species, and these data often give 61 insights into identity that are overlooked based on morphology alone (Hebert and Gregory, 62 2005). Plant DNA barcoding has been used for species discovery, reconstructing historical 63 vegetation types from frozen sediments, surveying environmental variation, and many other 64 research topics (reviewed in Hollingsworth et al., 2016). Despite the extensive uptake of 65 DNA barcoding, there are numerous reports of taxon groups where DNA barcodes do not 66 provide exact plant species identification, and where DNA barcode sequences are shared 67 among related species (Percy et al., 2014, Yan et al., 2015a, Yan et al., 2015b, Spooner, 68 2009). Identifying the causes of why DNA barcoding ‘fails’ is essential to help guide the 69 development of future DNA barcoding systems. If species discrimination is usually limited 70 by information content of the core barcoding loci, then improvements can be made by 71 extending the DNA barcode to harness variation across the whole plastid genome. In contrast, 72 if limits to species discrimination are caused by hybridisation, incomplete lineage sorting, and 73 polyploidy, then we may see no improvement with more plastid data, and future barcoding 74 systems will need to target the nuclear genome, as well as use new analytical methods to cope 75 with many independent loci (Coissac et al., 2016, Hollingsworth et al., 2016). As such, more 76 genetic studies of complex taxa groups are required in order to identify the underlying 77 evolutionary processes that can cause DNA barcoding to fail. In addition, the generation of 78 large data sets of DNA sequence data from multiple individuals of multiple species in such 79 groups also provide datasets that can shed light onto evolutionary relationships and 80 evolutionary divergence, without a need for the barcode markers to track species boundaries. 81 4 bioRxiv preprint doi: https://doi.org/10.1101/164681; this version posted July 17, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 82 Postglacial species radiations of taxonomically complex groups in Northern Europe are a case 83 where we may not expect a clear cut-off between intraspecific variation and interspecific 84 divergence and thus DNA barcoding may provide limited discriminatory power. Despite this, 85 DNA barcoding may still be valuable if used to identify evolutionary and ecological 86 processes that result in shared sequence variation. For example, many postglacial taxa are 87 characterised by a combination of: (1) recent postglacial speciation, (2) extensive 88 hybridisation, (3) frequent self-fertilization, (4) divergence involving polyploidy. Our 89 expectation is that factors 1 + 2 will cause DNA barcode sequences to be shared among 90 geographically proximate taxa, while 3 will cause barcodes to be population rather than 91 species-specific (Hollingsworth et al., 2011). Factor 4, polyploidy, will manifest as shared 92 haplotypes between recent polyploids and their parental progenitors, or deep haplotype 93 divergence in older polyploid groups, where ploidy act as a reproductive isolating barrier and 94 allows congeneric taxa to accumulate genetic differences. Many of these interacting factors 95 are common across taxonomically complex postglacial groups (Ennos, 2005), which include 96 the Arabidopsis arenosa complex (Schmickl et al., 2012), Cerastium (Brysting et al., 2007), 97 Epipactis (Squirrell et al., 2002) and Galium (Kolář et al., 2015). As such, the application of 98 DNA barcoding to such groups will not only reveal the prevalence of haplotype sharing and 99 the potential for species discrimination, but improve our understanding of processes 100 underlying shared variation. 101 102 One example of a taxonomically challenging group showing postglacial divergence is British 103 Euphrasia species. This group of 19 taxa are renowned for their difficult species 104 identification, and at present only a handful of experts can identify these species in the field. 105 Morphological species identification is difficult due to their small stature, combined with 106 species being defined by a complex suite of overlapping characters (Yeo, 1978). They are 5 bioRxiv preprint doi: https://doi.org/10.1101/164681; this version posted July 17, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 107 also generalist hemiparasites and thus phenotypes are plastic and depend upon host quality 108 (Svensson and Carlsson, 2004). DNA barcode-based identification could partly resolve these 109 identification issues, and lead to a greater understanding of species diversity and distributions
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